Comparative plastome analysis of Musaceae and new insights into phylogenetic relationships

Abstract

Background Musaceae is an economically important family consisting of 70-80 species. Elucidation of the interspecific relationships of this family is essential for a more efficient conservation and utilization of genetic resources for banana improvement. However, the scarcity of herbarium specimens and quality molecular markers have limited our understanding of the phylogenetic relationships in wild species of Musaceae. Aiming at improving the phylogenetic resolution of Musaceae, we analyzed a comprehensive set of 49 plastomes for 48 species/subspecies representing all three genera of this family. Results Musaceae plastomes have a relatively well-conserved genomic size and gene content, with a full length ranging from 166,782 bp to 172,514 bp. Variations in the IR borders were found to show phylogenetic signals to a certain extent in Musa. Codon usage bias analysis showed different preferences for the same codon between species and three genera and a common preference for A/T-ending codons. Among the two genes detected under positive selection (dN/dS > 1), ycf2 was indicated under an intensive positive selection. The divergent hotspot analysis allowed the identification of four regions (ndhF-trnL, ndhF, matK-rps16, and accD) as specific DNA barcodes for Musaceae species. Bayesian and maximum likelihood phylogenetic analyses using full plastome resulted in nearly identical tree topologies with highly supported relationships between species. The monospecies genus Musella is sister to Ensete, and the genus Musa was divided into two large clades, which corresponded well to the basic number of n = x = 11 and n = x =10/9/7, respectively. Four subclades were divided within the genus Musa. A dating analysis covering the whole Zingiberales indicated that the divergence of Musaceae family originated in the Palaeocene (59.19 Ma), and the genus Musa diverged into two clades in the Eocene (50.70 Ma) and then started to diversify from the late Oligocene (29.92 Ma) to the late Miocene. Two lineages (Rhodochlamys and Australimusa) radiated recently in the Pliocene /Pleistocene periods. Conclusions The plastome sequences performed well in resolving the phylogenetic relationships of Musaceae and generated new insights into its evolution. Plastome sequences provided valuable resources for population genetics and phylogenetics at lower taxon.

Hybridization, missing wild ancestors and the domestication of cultivated diploid bananas

“…These genomic results also suggested secondary diversification and dispersal of the ancestors of the others M. acuminata subspecies through the Malayan peninsula to Java, and then to New Guinea island and back to the southern Indo-Malayan region (Rouard et al, 2018). Using chloroplast sequences, Fu et al (2022) confirmed the early emergence of ssp. burmannica from the Indo-Burma region, as well as dispersal and emergence of the other subspecies towards Island South-East Asia and New Guinea but with a slightly different pattern.…”

“…Musa acuminata arose about 10 million years ago, probably in the northern Indo-Burma region (Janssens et al, 2016). Phylogenetic and phylogeographic studies performed on different markers obtained discordant results on its diversification and its dispersal at the intraspecific level (Janssens et al, 2016;Rouard et al, 2018;Fu et al, 2022). Whole genome sequences of four M. acuminata subspecies, ssp.…”

The Musa troglodytarum L. genome provides insights into the mechanism of non-climacteric behaviour and enrichment of carotenoids

“…Through chromosome rearrangement analysis of the T genome, we found that ancestral chromosomes 8 and 9 fused into modern chromosome 9. Phylogenetic analysis based on orthologous genes shows that the divergence time between M. troglodytarum and the ancestor of M. acuminata and M. schizocarpa was about 20.8 MYA, indicating a much earlier divergence time between Callimusa and Musa than previous reported 37.9-50.7 MYA [46][47][48]. This may be because of utilizing more informative characters to construct phylogentetic trees in genome-wide studies.…”

The banana genome hub: a community database for genomics in the Musaceae

“…The Zingiberales order evolution was shaped by lineage specific ancient whole genome duplications [ 7 , 22 ] and within the Musaceae , for which the crown age was estimated at 59.19 Ma [ 68 ], a large number of chromosome rearrangements occurred [ 24 , 69 ]. As an example, M. acuminata and M. balbisiana differ by a large translocation on chromosome1/3 and a large inversion on chromosome 5 [ 12 ].…”

“…We collected 16 publicly released Musaceae nuclear genome sequences (8 high-quality and 8 draft sequences) that were released publicly ( Table 1 ) as well as 91 chloroplast assemblies [ 68 , 71 – 75 ]. Functional annotations from InterPro were obtained using InterProScan [ 76 ].…”